Mitey Costly: Energetic Costs of Parasite Avoidance and Infection

Abstract

Parasites reduce host fitness via perturbations to host energy allocation, growth, survival, and reproduction. Here, we investigate the independent effects of parasite exposure and infection on host metabolic rate. Our study focuses on Drosophila hydei and a naturally occurring ectoparasitic mite, Macrocheles muscaedomesticae. We use flow-through respirometry to measure the metabolic rate of flies during the period of exposure (preinfection) and during mite attachment. Flies were exposed to mites either indirectly (through a mesh screen) or directly, allowing for physical contact between the fly and the mite. We predicted that fly metabolic rate would increase with the level of parasite exposure: unexposed flies < flies with indirect exposure to mites < flies with direct contact with mites < flies actively infected with mites. As expected, flies indirectly exposed to but not in direct contact with mites produced 70% more CO than unexposed flies. Flies in direct contact with mites produced 35% more CO than flies with indirect contact, and this was more than double the amount of CO produced by unexposed flies. However, infected flies-those actually carrying mites-did not produce significantly more CO than uninfected flies. Our results show that simply being exposed to mites, either indirectly or directly, was sufficient to elicit a response from the host in terms of elevated CO production. Our results show that the costs of parasitism can potentially extend beyond the physiological costs of infection per se to include the energetic costs associated with parasite avoidance. Although studies have shown energetic costs associate with predator-avoidance behaviors, no study to our knowledge has measured the metabolic cost of parasite avoidance.

An Integrated Landscape of Fear and Disgust: The Evolution of Avoidance Behaviors Amidst a Myriad of Natural Enemies

“…As stated above, if the level of risk varies more over time, victims may evolve plastic traits to allocate energy responsively toward avoidance behaviors depending on perceived risk ( Figure 1C). For example, the metabolic rate in Drosophila flies increases when they are either indirectly or directly exposed to parasitic mites, but to different degrees, suggesting that the avoidance behaviors of the fly may have evolved to contend with different levels of risk imposed by the enemy (Luong et al, 2017).…”

A brain‐infecting parasite impacts host metabolism both during exposure and after infection is established

“…For instance, it may impact the host's overall energetic budget, given the frequency with which killifish naturally encounter cercariae in the wild (see below). In another system, Drosophila flies exposed to ectoparasitic mites also exhibit an increased metabolic rate (Luong et al., 2017), providing evidence that the observed changes in metabolic rate with acute parasite exposure are likely relevant for a wide range of host and parasite types.…”

“…These costs arise from several sources, including direct energy consumption by parasites, repairing or replacing damaged tissue or mounting immune responses (Sadd & Schmid‐Hempel, 2009; Walkey & Meakings, 1970). However, even before infection is established, parasites may metabolically impact their hosts if the hosts respond to the presence of parasite infectious stages (Luong et al., 2017). Although studies in a range of taxa have quantified how established infection impacts host metabolic rate (Robar et al., 2011), little work has examined the metabolic consequences of the host's response to initial parasite exposure (i.e.…”

“…Although studies in a range of taxa have quantified how established infection impacts host metabolic rate (Robar et al., 2011), little work has examined the metabolic consequences of the host's response to initial parasite exposure (i.e. Luong et al., 2017; Voutilainen et al., 2008) or compared these effects to the metabolic impacts of established parasite infection. Furthermore, to the best of our knowledge, no studies have tested if the metabolic response to parasite exposure is modulated by previous infection history, which would be particularly relevant for energy metabolism in systems where hosts frequently encounter infectious parasite stages.…”

“…Similar to the ‘ecology of fear’ described for predator–prey relationships (reviewed by Buck et al., 2018; Raffel et al., 2008), after detection of infectious stages, hosts may minimize infection risk by modifying activity, changing social behaviour or physically dislodging attacking parasites (James et al., 2008; Stumbo et al., 2012), all of which can increase metabolic rate (Speakman & Selman, 2003). Hosts can also exhibit physiological signs of stress following exposure to infectious parasite stages, including changes in ventilation, respiration and heart rates (Laitinen et al., 1996; Luong et al., 2017; Voutilainen et al., 2008). Such behavioural and physiological responses may also be learned or developed following initial parasite exposures, which could result in amplified host responses to subsequent encounter with the same parasite.…”